The joint evolution of mating system, floral traits and life history in Clarkia (Onagraceae): Genetic constraints vs. independent evolution

Journal of Evolutionary Biology

Volumn 20, Issue 6, 2007, Pages 2200-2218

  Dudley, L S ^a,c   Mazer, S J ^a   Galusky, P ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Riverside Community College   (United States)

^c UNIVERSITY OF CHILE   (Chile)

Author keywords

Autogamy; Clarkia; Genetic correlation; Life history; Protandry; Reproductive maturity; Successive flower development

Indexed keywords

ANGIOSPERM; AUTOGAMY; DIVERGENCE; EVOLUTION; LIFE HISTORY TRAIT; OUTCROSSING; PLEIOTROPY; REPRODUCTIVE STRATEGY; REPRODUCTIVE SUCCESS; SELECTION; SEXUAL MATURITY;

ARTICLE; CLARKIA; CLASSIFICATION; EVOLUTION; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY;

CLARKIA; EVOLUTION; FLOWERS;

CLARKIA; CLARKIA EXILIS; CLARKIA UNGUICULATA; CLARKIA XANTIANA; ONAGRACEAE;

EID: 35448985024     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2007.01421.x     Document Type: Article

References (88)

1. Allen, G.A., Gottlieb, L.D. Ford, V.S. 1991. Electrophoretic evidence for the independent origins of two self-pollinating subspecies of Clarkia concinna (Onagraceae). Can. J. Bot. 69 : 2299 2301.
2. Armbruster, W.S. 1985. Patterns of character divergence and the evolution of reproductive ecotypes of Dalechampia scandens (Euphorbiaceae). Evolution 39 : 733 752.
3. Armbruster, W.S. 1988. Multilevel comparative analysis of the morphology, function, and evolution of Dalechampia blossoms. Ecology 69 : 1746 1761.
4. Armbruster, W.S. Schwaegerle, K.E. 1996. Causes of covariation of phenotypic traits among populations. J. Evol. Biol. 9 : 261 276.
5. Armbruster, W.S., Mulder, C.P.H., Baldwin, B.G., Kalisz, S., Wessa, B. Nute, H. 2002. Comparative analysis of late floral development and mating-system evolution in Tribe Collinsieae (Scrophulariaceae S.L.). Am. J. Bot. 89 : 37 49.
6. Arnold, S.J. 1992. Constraints on phenotypic evolution. Am. Nat. 140 : S85 S107.
7. Arroyo, M.T.K. 1973. Chiasma frequency evidence on evolution of autogamy in Limnanthes floccosa (Limnanthaceae). Evolution 27 : 679 688.
8. Ashman, T.-L. Majetic, C.J. 2006. Genetic constraints on floral evolution: a review and evaluation of patterns. Heredity 96 : 343 352.
9. Ashman, T.-L. Schoen, D.J. 1997. The cost of floral longevity in Clarkia tembloriensis: an experimental investigation. Evol. Ecol. 11 : 289 300.
10. Baker, H.G. 1955. Self-compatibility and establishment after ''long-distance" dispersal. Evolution 9 : 347 349.
11. Baker, H.G. 1967. Support for Baker's law-as a rule. Evolution 21 : 853 856.
12. Brodie, E.D. 1989. Genetic correlations between morphology and antipredator behavior in natural populations of the garter snake Thamnophis ordinoides. Nature 342 : 542 543.
13. Brodie, E.D. 1992. Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46 : 1284 1298.
14. Conner, J.K. Sterling, A. 1995. Testing hypotheses of functional relationships: a comparative survey of correlation patterns among floral traits in five insect-pollinated plants. Am. J. Bot. 82 : 1399 1406.
15. Cugen, J., Acheroy, M., Loutfi, A.L., Petit, D. Vernet, P. 1989. Breeding system differentiation in Arrhenatherum elatius populations: evolution toward selfing Evol. Trends Plants 3 : 17 24.
16. Damgaard, C. Abbott, R.J. 1995. Positive correlations between selfing rate and pollen-ovule ratio within plant populations. Evolution 49 : 214 217.
17. Diggle, P.K. 1992. Development and the evolution of plant reproductive characters. In : Ecology and Evolution of Plant Reproduction (R. Wyatt, ed. pp. 326 355. Chapman and Hall, New York, NY.
18. Eckhart, V.M. Geber, M.A. 1999. Character variation and geographic distribution of Clarkia xantiana (Onagraceae): flowers and phenology distinguish two subspecies. Madroño 46 : 117 125.
19. Eckhart, V.M. Geber, M.A. 2000. Character variation and geographic range in Clarkia xantiana (Onagraceae): breeding system and phenology distinguish two common subspecies. Madroño 46 : 117 125.
20. Eckhart, V.M., Geber, M.A. Jonas, C.S. 1996. Developmental controls of flowering-time evolution in Clarkia (Onagraceae). Am. J. Bot. 83 : 81 (abstracts).
21. Eckhart, V.M., Geber, M.A. McGuire, C.M. 2004. Experimental studies of adaptation in Clarkia xantiana: I. Sources of trait variation across a subspecies border. Evolution 58 : 59 70.
22. Ehlers, B.K. 1999. Variation in fruit set within and among natural populations of the self-incompatible herb Centaurea scabiosa (Asteraceae). Nord. J. Bot. 19 : 653 663.
23. Elle, E. Carney, R. 2003. Reproductive assurance varies with flower size in Collinsia parviflora (Scrophulariaceae). Am. J. Bot. 90 : 888 896.
24. Fausto, J.A., Eckhart, V.M. Geber, M.A. 2001. Reproductive assurance and the evolutionary ecology of self-pollination in Clarkia xantiana (Onagraceae). Am. J. Bot. 88 : 1794 1800.
25. Fenster, C.B. Carr, D.E. 1997. Genetics of sex allocation in Mimulus (Scrophulariaceae). J. Evol. Biol. 10 : 641 661.
26. Fenster, C.B., Diggle, P.K., Barrett, S.C.H. Ritland, K. 1995. The genetics of floral development differentiating two species of Mimulus (Scrophulariaceae). Heredity 74 : 258 266.
27. Fisher, R.A. 1941. Average excess and average effect of a gene substitution. Ann. Eugen. 11 : 53 63.
28. Fishman, L. Stratton, D.A. 2004. The genetics of floral divergence and postzygotic barriers between outcrossing and selfing populations of Arenaria uniflora (Caryophyllaceae). Evolution 58 : 296 307.
29. Gallardo, R., Dominguez, E. Munoz, J.M. 1994. Pollen-ovule ratio, pollen size, and breeding system in Astragalus (Fabaceae) subgenus Epiglottis: a pollen and seed allocation approach. Am. J. Bot. 81 : 1611 1619.
30. Geber, M.A. Eckhart, V.M. 2005. Experimental studies of adaptation in Clarkia xantiana: II. Fitness variation across a subspecies border. Evolution 59 : 521 531.
31. Gómez, J.M. 2002. Self-pollination in Euphrasia willkommii Freyn (Scrophulariaceae), an endemic species from the alpine of the Sierra Nevada (Spain). Plant Syst. Evol. 232 : 63 71.
32. Groom, M.J. 1998. Allee effects limit population viability of an annual plant. Am. Nat. 151 : 487 496.
33. Guerrant, E.O. Jr. 1984. The role of ontogeny in the evolution and ecology of selected species of Delphinium and Limnanthes. University of California, Berkeley, CA.
34. Guerrant, E.O. Jr. 1988. Heterochrony in plants: the intersection of evolution, ecology, and ontogeny. In : Heterochrony in Evolution: a Multidisciplinary Approach (M. L. McKinney, ed. pp. 111 134. Plenum Press, New York.
35. Guerrant, E.O. 1989. Early maturity, small flowers and autogamy: a developmental connection. In : The Evolutionary Ecology of Plants (J. H. Bock Y. B. Linhart, eds pp. 61 84. Westview Press, Boulder, CO.
36. Hayes, C.N., Winsor, J.A. Stephenson, A.G. 2005. Multigenerational effects of inbreeding in Cucurbita pepo ssp. texana (Cucurbitaceae). Evolution 59 : 276 286.
37. Herrera, J. 2001. The variability of organs differentially involved in pollination, and correlations of traits in Genisteae (Leguminosae: Papilionoideae). Ann. Bot. 88 : 1027 1037.
38. Hill, J.P., Lord, E.M. Shaw, R.G. 1992. Morphological and growth rate differences among outcrossing and self-pollinating races of Arenaria uniflora (Caryophyllaceae). J. Evol. Biol. 5 : 559 573.
39. Holeski, L.M. Kelly, J.K. 2006. Mating system and the evolution of quantitative traits: an experimental study of Mimulus guttatus. Evolution 60 : 711 723.
40. Holsinger, K.E. 1996. Pollination biology and the evolution of mating systems in flowering plants. In : Evolutionary Biology (M. K. Hecht, R. J. Macintyre M. T. Clegg, eds pp. 107 149. Plenum Press, New York.
41. Holsinger, K.E. 2000. Reproductive systems and evolution in vascular plants. Proc. Natl Acad. Sci. U.S.A. 97 : 7037 7042.
42. Holtsford, T.P. Ellstrand, N.C. 1992. Genetic and environmental variation in floral traits affecting outcrossing rate in Clarkia tembloriensis (Onagraceae). Evolution 46 : 216 225.
43. Jain, S.K. 1976. Evolution of inbreeding in plants. Annu. Rev. Ecol. Syst. 7 : 469 495.
44. Jonas, C.S. Geber, M.A. 1999. Variation among populations of Clarkia unguiculata (Onagraceae) along altitudinal and latitudinal gradients. Am. J. Bot. 86 : 333 343.
45. Kelly, J.K. 1999. Response to selection in partially self-fertilizing populations: II. Selection on multiple traits. Evolution 53 : 350 357.
46. Lande, R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33 : 402 416.
47. Lande, R. 1984. The genetic correlation between characters maintained by selection, linkage and inbreeding. Genet. Res. 44 : 309 320.
48. Lewis, H. Lewis, M.E. 1955. The Genus Clarkia. University of California Press, Berkeley, CA.
49. Lewis, H. Raven, P.H. 1958. Rapid evolution in Clarkia. Evolution 12 : 319 336.
50. Lloyd, D.G. 1965. Evolution of self-compatibility and racial differentiation in Leavenworthia (Cruciferae). Harv. Univ. Gray Herb. Contr. 195 : 1 134.
51. Lloyd, D.G. 1992. Self- and cross-fertilization in plants: II. The selection of self-fertilization. Int. J. Plant Sci. 153 : 370 380.
52. Maad, J. 2000. Phenotypic selection in hawkmoth-pollinated Platanthera bifolia: targets and fitness surfaces. Evolution 54 : 112 123.
53. Mazer, S.J., Lowry, D.E. Hansen, T. 2003. Effects of nutrient availability on primary sexual traits and their response to selection in Spergularia marina (Caryophyllaceae). J. Evol. Biol. 16 : 767 778.
54. Mazer, S.J., Paz, H. Bell, M.D. 2004. Life history, floral development, and mating system in Clarkia xantiana (Onagraceae): do floral and whole-plant rates of development evolve independently Am. J. Bot. 91 : 2041 2050.
55. Mazer, S.J., Delesalle, V.A. Paz, H. 2007. Evolution of mating system and the genetic covariance between male and female investment in Clarkia (Onagraceae): selfing opposes the evolution of trade-offs. Evolution 61 : 83 98.
56. Moeller, D.A. 2004. Facilitative interactions among plants via shared pollinators. Ecology 85 : 3289 3301.
57. Moeller, D.A. 2005. Pollinator community structure and sources of spatial variation in plant-pollinator interactions in Clarkia xantiana ssp. xantiana. Oecologia 142 : 28 37.
58. Moeller, D.A. Geber, M.A. 2005. Ecological context of the evolution of self-pollination in Clarkia xanitiana: population size, plant communities and reproductive assurance. Evolution 59 : 786 799.
59. Moore, D.M. Lewis, H. 1965. The evolution of self-pollination in Clarkia xantiana. Evolution 19 : 104 114.
60. Morgan-Richards, M. Wolff, K. 1999. Genetic structure and differentiation of Plantago major reveals a pair of sympatric sister species. Mol. Ecol. 8 : 1027 1036.
61. Petanidou, T., Ellis-Adam, A.C., den Nijs, J.C.M. Oostermeijer, J.G.B. 1998. Pollination ecology of Gentianella uliginosa, a rare annual of the Dutch coastal dunes. Nord. J. Bot. 18 : 537 548.
62. Runions, C.J. Geber, M.A. 2000. Evolution of the self-pollinating flower in Clarkia xantiana (Onagraceae): I. Size and development of floral organs. Am. J. Bot. 87 : 1439 1451.
63. Schemske, D.W. 1978. Sexual reproduction in an Illinois population of Sanguinaria canadensis L. Am. Midl. Nat. 100 : 261 268.
64. Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50 : 1766 1774.
65. Schoen, D.J. 1982. The breeding system of Gilia achilleifolia: variation in floral characteristics and outcrossing rate. Evolution 36 : 352 360.
66. Schoen, D.J., Morgan, M.T. Bataillon, T. 1996. How does self-pollination evolve? Inferences from floral ecology and molecular genetic variation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351 : 1281 1290.
67. Shaw, R.G., Byers, D.L. Shaw, F.H. 1998. Genetic components of variation in Nemophila menziesii undergoing inbreeding: morphology and flowering time. Genetics 150 : 1649 1661.
68. Sinervo, B. Svensson, E. 2002. Correlational selection and the evolution of genomic architecture. Heredity 89 : 329 338.
69. Sinervo, B., Svensson, E. Comendant, T. 2000. Density cycles and offspring quantity and quality game driven by natural selection. Nature 406 : 985 988.
70. Stewart, H.M. Canne-Hilliker, J.M. 1998. Floral development of Agalinis neoscotica, Agalinis paupercula var. borealis, and Agalinis purpurea (Scrophulariaceae): implications for taxonomy and mating system. Int. J. Plant Sci. 159 : 418 439.
71. Strid, A. 1969. Evolutionary trends in breeding system of Nigella (Ranunculaceae). Bot. Not. 122 : 382 397.
72. Stucky, J.M. 1985. Pollination systems of sympatric Ipomoea hederacea and Ipomoea purpurea and the significance of interspecific pollen flow. Am. J. Bot. 72 : 32 43.
73. Svensson, E., Sinervo, B. Comendant, T. 2001. Condition, genotype-by-environment interaction and correlational selection in lizard life-history morphs. Evolution 55 : 2053 2069.
74. Travers, S.E. Mazer, S.J. 2000. The absence of cryptic self-incompatibility in Clarkia unguiculata (Onagraceae). Am. J. Bot. 87 : 191 196.
75. Turelli, M. 1988. Phenotypic evolution, constant covariances and the maintenance of additive variance. Evolution 42 : 1342 1347.
76. Vasek, F.C. 1964. Evolution of Clarkia unguiculata derivatives adapted to relatively xeric environments. Evolution 18 : 26 42.
77. Vasek, F.C. 1965. Outcrossing in natural populations: II. Clarkia unguiculata. Evolution 19 : 152 156.
78. Vasek, F.C. 1968. Relationships of two ecologically marginal, sympatric Clarkia populations. Am. Nat. 102 : 25 40.
79. Vasek, F.C. Harding, J. 1976. Outcrossing in natural populations: V. Analysis of outcrossing, inbreeding, and selection in Clarkia exilis and Clarkia tembloriensis. Evolution 30 : 403 411.
80. Vasek, F.C. Sauer, R.H. 1971. Seasonal progression of flowering in Clarkia. Ecology 52 : 1038 1045.
81. Vasek, F.C. Weng, V. 1988. Breeding systems of Clarkia sect. Phaeostoma (Onagraceae): I. Pollen-ovule ratios. Syst. Bot. 13 : 336 350.
82. Whitlock, M.C. Fowler, K. 1999. The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics 152 : 345 353.
83. Wilkinson, G.S., Fowler, K. Partridge, L. 1990. Resistance of genetic correlation structure to directional selection in Drosophila melanogaster. Evolution 44 : 1990 2003.
84. Willis, J.H. 1996. Measures of phenotypic selection are biased by partial inbreeding. Evolution 50 : 1501 1511.
85. Wyatt, R. 1984a. The evolution of self-pollination in granite outcrop species of Arenaria (Caryophyllaceae): 1. Morphological correlates. Evolution 38 : 804 816.
86. Wyatt, R. 1984b. Evolution of self-pollination in granite outcrop species of Arenaria (Caryophyllaceae): III. Reproductive effort and pollen-ovule ratios. Syst. Bot. 9 : 432 440.
87. Wyatt, R. 1986. Ecology and evolution of self-pollination in Arenaria uniflora (Caryophyllaceae). J. Ecol. 74 : 403 418.
88. Zeng, Z.-B. 1988. Long-term correlated response, interpopulation covariation, and interspecific allometry. Evolution 42 : 363 374.